DOCSLIB.ORG

Dynamical Modules in Metabolism, Cell and Developmental Biology Johannes Jaeger1,2 Nick Monk3*

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Dynamical Modules in Metabolism, Cell and Developmental Biology Johannes Jaeger1,2 Nick Monk3* Dynamical Modules in Metabolism, Cell and Developmental Biology Johannes Jaeger1,2 Nick Monk3* (1) Complexity Science Hub (CSH) Vienna, Josefstädter Straße 39, 1080 Vienna, Austria (2) School of Mathematics and Statistics, University of Sheffield, Hicks Building, Sheffield S3 7RH, UK * Corresponding author: [email protected], +44 114 222 3857 Abstract Modularity is an essential feature of any adaptive complex system. Phenotypic traits are modules in the sense that they have a distinguishable structure or function, which can vary (quasi-)independently from its context. Since all phenotypic traits are the product of some underlying regulatory dynamics, the generative processes that constitute the genotype- phenotype map must also be functionally modular. Traditionally, modular processes have been identified as structural modules in regulatory networks. However, structure only constrains, but does not determine the dynamics of a process. Here, we propose an alternative approach that decomposes the behaviour of a complex regulatory system into elementary activity-functions. Modular activities can occur in networks that show no structural modularity, making dynamical modularity more widely applicable than structural decomposition. Furthermore, the behaviour of a regulatory system closely mirrors its functional contribution to the outcome of a process, which makes dynamical modularity particularly suited for functional decomposition. We illustrate our approach with numerous examples from the study of metabolism, cellular processes, as well as development and pattern formation. We argue that dynamical modules provide a shared conceptual foundation for developmental and evolutionary biology, and serve as the foundation for a new account of process homology. Keywords modularity, dynamical systems, activity-function, regulatory networks, metabolic control, systems biology 1 1. Introduction: the Modular Epigenotype Organisms are characterised by distinguishable metabolic, physiological, developmental, morphological, and behavioral traits. These phenotypic traits are modular, able to evolve in a quasi-independent manner (Fig. 1A) (Lewontin, 1970, 1974). Herbert Simon (1962, 1973), was among the first to point out that such “near-decomposability” must be a fundamental and universal property of adaptive complex systems. Similar ideas are implicit in Stuart Kauffman’s notion of biological systems being poised on “the edge of chaos”—with modular “islands of chaos” among a large percolating component of “order” (Kauffman, 1993; see Jaeger & Monk, 2021, for a detailed discussion). By limiting the off-target (pleiotropic) effects of mutations, a modular architecture enables evolution through targeted selection for specific trait functions. Wings are adapted for flying, and legs for walking, because fore- and hind-limbs in aerial vertebrates can evolve quasi-independently: even though they share a common underlying structure, their shape and size can be altered in different directions (Fig. 1A). It is widely accepted today that trait modularity is a fundamental prerequisite for evolvability, defined as the capacity of a system to generate adaptive change (Dawkins 1989; Wagner & Altenberg 1996; Pigliucci 2008). Consistent with this, modular traits are ubiquitous in evolving organisms. They have been described at many different levels of organisation, from behavioral patterns to morphological characters to intercellular signaling pathways to cis-regulatory sequences involved in gene regulation (Schlosser & Wagner, 2004; Callebaut & Rasskin-Gutman, 2005). All biological traits are generated by some underlying regulatory dynamics (Jaeger et al., 2012; Jaeger & Monk, 2014; DiFrisco & Jaeger, 2021). These generative processes constitute the epigenotype of the organism (Waddington 1942, 1953, 1957; Goodwin, 1982; Oster & Alberch, 1982), which is often represented as a complex mapping from genotype to phenotype (Fig. 1B) (Burns 1970; Alberch 1991; Pigliucci 2010). If we are to properly understand the evolutionary sources of phenotypic variability—the substrate on which natural selection can act—we must study the structure of this mapping in a mechanistic manner (Jaeger et al., 2012; Jaeger & Monk, 2014, 2021; DiFrisco & Jaeger, 2019, 2020). What we are ultimately interested in are the causal processes that generate the variational properties of an adaptive and evolvable complex system. 2 Figure 1: Modularity of the genotype-phenotype map. (A) Phenotypic traits are modular. They are distinguishable in terms of either structure or function, and are able to evolve in quasi-independent ways. An example is the specialisation of vertebrate fore-limbs into arms and wings. (B) This implies that the processes that generate these traits—the epigenotype of the organism, which mediates the mapping from genotype to phenotype—must also be modular and dissociable (at least to some extent). Adapted from Jaeger & Monk (2021). See text for details. An important first step in this direction is to recognise that the quasi-independence of modular traits necessitates a modular structure of the underlying epigenotype (Fig. 1). The processes that generate traits must themselves be modular or dissociable (at least to some extent) for those traits to be able to vary quasi-independently (Needham, 1933). Therefore, it should be possible to map the source of variation in specific traits back to variability in specific modular subsystems of the epigenotype. This is not a trivial task and the precise nature of epigenetic modularity remains elusive, which is the problem we tackle in this paper. Elsewhere, we have developed a detailed theoretical account of dynamic modularity, which allows us to decompose the genotype-phenotype map into dissociable causal processes (Jaeger & Monk, 2021). Here, we briefly reiterate the main features of our account, illustrating it with a range of examples. In the next section, we start with an overview of the different types of modules one can identify in biological systems, comparing the advantages and drawbacks of 3 each kind of modular decomposition. We then continue by introducing our own dynamical and activity-based notion of modularity. The examples we provide represent regulatory processes from the fields of metabolism, cell and developmental biology. We conclude by discussing some of the wider implications of dynamical modularity, especially in evolutionary biology. 2. Kinds of Modules Modules, defined in the broadest sense, are parts, components, or subsystems of a larger system that possess a specific functional or structural identity (Moss, 2001). They must persist long enough to exert their effect (Callebaut, 2005). Modules themselves can consist of different kinds of entities: physical objects or structures, regulatory pathways or processes, and even types of behaviour as we shall show here. Modularity in complex systems is always a matter of degree (Wagner & Altenberg, 1996). On the one hand, all modules interact with their context— usually in a structured and hierarchical way. On the other hand, a system is modular to the extent to which its components operate according to their own intrinsically determined principles (Callebaut, 2005). In other words, modules exhibit internal causal cohesion coupled with a certain degree of autonomy from their context (Collier 1988, 2004; DiFrisco, 2018). This means that modules can be reused, since they are able to operate robustly across a certain range of circumstances (Mireles and Conrad, 2018). There are many different kinds of modules, and various methods to distinguish them. One approach classifies modules according to their biological context, e.g. developmental vs. evolutionary modules (Raff, 1996; Brandon, 1999; von Dassow & Munro, 1999; Bolker, 2000; Callebaut, 2005; Wagner et al. 2007). Another type of classification is based on what kind of entities a module is composed of: morphological modules consist of physical structures, developmental modules of processes (Winther, 2001; Callebaut, 2005). Here, we will focus on how modularity is relative to the specific way in which a system is decomposed into parts or subsystems. Each such decomposition provides a different perspective on a complex system (Wimsatt, 2007). Decompositions based on functional, regulatory, structural, or variational criteria result in modules with different properties and biological applications (Fig. 2) (see Jaeger & Monk, 2021, for a more detailed discussion). We will briefly review each of these in turn, before we move on to modules that are defined in terms of their dynamical behaviour. 4 Figure 2: Different kinds of modules. (A) Variational modules are distinguished by their ability to vary quasi-independently of the rest of the system. In the example shown here, the shape, size, and colour of ears and eyes can vary independently. These two morphological traits are therefore variational modules. (B) Functional modules are defined by the use-function their components contribute to. Shown here are the hierarchical layers of the Drosophila segmentation gene hierarchy. Genes in each layer cause similar kinds of phenotypes when mutated. They also show similarities in gene expression patterns (as shown here schematically). Downward arrows indicate hierarchical regulatory interactions; circular arrows indicate complex cross-regulation within each layer. (C) Structural motifs come in different flavours. Network motifs (left): small subnetworks that are statistically enriched above a given threshold (dashed line)
Load more

Recommended publications
  • The Polyp and the Medusa Life on the Move
    The Polyp and the Medusa Life on the Move Millions of years ago, unlikely pioneers sparked a revolution. Cnidarians set animal life in motion. So much of what we take for granted today began with Cnidarians. FROM SHAPE OF LIFE The Polyp and the Medusa Life on the Move Take a moment to follow these instructions: Raise your right hand in front of your eyes. Make a fist. Make the peace sign with your first and second fingers. Make a fist again. Open your hand. Read the next paragraph. What you just did was exhibit a trait we associate with all animals, a trait called, quite simply, movement. And not only did you just move your hand, but you moved it after passing the idea of movement through your brain and nerve cells to command the muscles in your hand to obey. To do this, your body needs muscles to move and nerves to transmit and coordinate movement, whether voluntary or involuntary. The bit of business involved in making fists and peace signs is pretty complex behavior, but it pales by comparison with the suites of thought and movement associated with throwing a curve ball, walking, swimming, dancing, breathing, landing an airplane, running down prey, or fleeing a predator. But whether by thought or instinct, you and all animals except sponges have the ability to move and to carry out complex sequences of movement called behavior. In fact, movement is such a basic part of being an animal that we tend to define animalness as having the ability to move and behave.
    [Show full text]
  • Animal Origins and the Evolution of Body Plans 621
    Animal Origins and the Evolution 32 of Body Plans In 1822, nearly forty years before Darwin wrote The Origin of Species, a French naturalist, Étienne Geoffroy Saint-Hilaire, was examining a lob- ster. He noticed that when he turned the lobster upside down and viewed it with its ventral surface up, its central nervous system was located above its digestive tract, which in turn was located above its heart—the same relative positions these systems have in mammals when viewed dorsally. His observations led Geoffroy to conclude that the differences between arthropods (such as lobsters) and vertebrates (such as mammals) could be explained if the embryos of one of those groups were inverted during development. Geoffroy’s suggestion was regarded as preposterous at the time and was largely dismissed until recently. However, the discovery of two genes that influence a sys- tem of extracellular signals involved in development has lent new support to Geof- froy’s seemingly outrageous hypothesis. Genes that Control Development A A vertebrate gene called chordin helps to establish cells on one side of the embryo human and a lobster carry similar genes that control the development of the body as dorsal and on the other as ventral. A probably homologous gene in fruit flies, called axis, but these genes position their body sog, acts in a similar manner, but has the opposite effect. Fly cells where sog is active systems inversely. A lobster’s nervous sys- become ventral, whereas vertebrate cells where chordin is active become dorsal. How- tem runs up its ventral (belly) surface, whereas a vertebrate’s runs down its dorsal ever, when sog mRNA is injected into an embryo (back) surface.
    [Show full text]
  • Giraffe Stature and Neck Elongation: Vigilance As an Evolutionary Mechanism
    biology Review Giraffe Stature and Neck Elongation: Vigilance as an Evolutionary Mechanism Edgar M. Williams Faculty of Life Sciences and Education, University of South Wales, Wales CF37 1DL, UK; [email protected]; Tel.: +44-1443-483-893 Academic Editor: Chris O’Callaghan Received: 1 August 2016; Accepted: 7 September 2016; Published: 12 September 2016 Abstract: Giraffe (Giraffa camelopardalis), with their long neck and legs, are unique amongst mammals. How these features evolved is a matter of conjecture. The two leading ideas are the high browse and the sexual-selection hypotheses. While both explain many of the characteristics and the behaviour of giraffe, neither is fully supported by the available evidence. The extended viewing horizon afforded by increased height and a need to maintain horizon vigilance, as a mechanism favouring the evolution of increased height is reviewed. In giraffe, vigilance of predators whilst feeding and drinking are important survival factors, as is the ability to interact with immediate herd members, young and male suitors. The evidence regarding giraffe vigilance behaviour is sparse and suggests that over-vigilance has a negative cost, serving as a distraction to feeding. In woodland savannah, increased height allows giraffe to see further, allowing each giraffe to increase the distance between its neighbours while browsing. Increased height allows the giraffe to see the early approach of predators, as well as bull males. It is postulated that the wider panorama afforded by an increase in height and longer neck has improved survival via allowing giraffe to browse safely over wider areas, decreasing competition within groups and with other herbivores.
    [Show full text]
  • The Cambrian Explosion: a Big Bang in the Evolution of Animals
    The Cambrian Explosion A Big Bang in the Evolution of Animals Very suddenly, and at about the same horizon the world over, life showed up in the rocks with a bang. For most of Earth’s early history, there simply was no fossil record. Only recently have we come to discover otherwise: Life is virtually as old as the planet itself, and even the most ancient sedimentary rocks have yielded fossilized remains of primitive forms of life. NILES ELDREDGE, LIFE PULSE, EPISODES FROM THE STORY OF THE FOSSIL RECORD The Cambrian Explosion: A Big Bang in the Evolution of Animals Our home planet coalesced into a sphere about four-and-a-half-billion years ago, acquired water and carbon about four billion years ago, and less than a billion years later, according to microscopic fossils, organic cells began to show up in that inert matter. Single-celled life had begun. Single cells dominated life on the planet for billions of years before multicellular animals appeared. Fossils from 635,000 million years ago reveal fats that today are only produced by sponges. These biomarkers may be the earliest evidence of multi-cellular animals. Soon after we can see the shadowy impressions of more complex fans and jellies and things with no names that show that animal life was in an experimental phase (called the Ediacran period). Then suddenly, in the relatively short span of about twenty million years (given the usual pace of geologic time), life exploded in a radiation of abundance and diversity that contained the body plans of almost all the animals we know today.
    [Show full text]
  • Defining Phyla: Evolutionary Pathways to Metazoan Body Plans
    EVOLUTION & DEVELOPMENT 3:6, 432-442 (2001) Defining phyla: evolutionary pathways to metazoan body plans Allen G. Collins^ and James W. Valentine* Museum of Paleontology and Department of Integrative Biology, University of California, Berkeley, CA 94720, USA 'Author for correspondence (email: [email protected]) 'Present address: Section of Ecology, Befiavior, and Evolution, Division of Biology, University of California, San Diego, La Jolla, CA 92093-0116, USA SUMMARY Phyla are defined by two sets of criteria, one pothesis of Nielsen; the clonal hypothesis of Dewel; the set- morphological and the other historical. Molecular evidence aside cell hypothesis of Davidson et al.; and a benthic hy- permits the grouping of animals into clades and suggests that pothesis suggested by the fossil record. It is concluded that a some groups widely recognized as phyla are paraphyletic, benthic radiation of animals could have supplied the ances- while some may be polyphyletic; the phyletic status of crown tral lineages of all but a few phyla, is consistent with molecu- phyla is tabulated. Four recent evolutionary scenarios for the lar evidence, accords well with fossil evidence, and accounts origins of metazoan phyla and of supraphyletic clades are as- for some of the difficulties in phylogenetic analyses of phyla sessed in the light of a molecular phylogeny: the trochaea hy- based on morphological criteria. INTRODUCTION Molecules have provided an important operational ad- vance to addressing questions about the origins of animal Concepts of animal phyla have changed importantly from phyla. Molecular developmental and comparative genomic their origins in the six Linnaean classis and four Cuvieran evidence offer insights into the genetic bases of body plan embranchements.
    [Show full text]
  • Modularity in Animal Development and Evolution: Elements of a Conceptual Framework for Evodevo
    JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 285:307–325 (1999) Modularity in Animal Development and Evolution: Elements of a Conceptual Framework for EvoDevo GEORGE VON DASSOW*AND ED MUNRO Department of Zoology, University of Washington, Seattle, Washington 98195-1800 ABSTRACT For at least a century biologists have been talking, mostly in a black-box sense, about developmental mechanisms. Only recently have biologists succeeded broadly in fishing out the contents of these black boxes. Unfortunately the view from inside the black box is almost as obscure as that from without, and developmental biologists increasingly confront the need to synthesize known facts about developmental phenomena into mechanistic descriptions of com- plex systems. To evolutionary biologists, the emerging understanding of developmental mecha- nisms is an opportunity to understand the origins of variation not just in the selective milieu but also in the variability of the developmental process, the substrate for morphological change. Ultimately, evolutionary developmental biology (EvoDevo) expects to articulate how the diversity of organic form results from adaptive variation in development. This ambition demands a shift in the way biologists describe causality, and the central problem of EvoDevo is to understand how the architecture of development confers evolvability. We argue in this essay that it makes little sense to think of this question in terms of individual gene function or isolated morphometrics, but rather in terms of higher-order modules such as gene networks and homologous characters. We outline the conceptual challenges raised by this shift in perspective, then present a selection of case studies we believe to be paradigmatic for how biologists think about modularity in devel- opment and evolution.
    [Show full text]
  • 2 Neurobiological View of Plants and Their Body Plan 21
    Neurobiological View of Plants 2 and Their Body Plan František Baluška, Dieter Volkmann, Andrej Hlavacka, Stefano Mancuso, Peter W. Barlow Abstract All principal metabolic biochemical pathways are conserved in animal and plant cells. Besides this, plants have been shown to be identical to animals from several other rather unexpected perspectives. For their reproduction, plants use identical sexual processes based on fusing sperm cells and oocytes. Next, plants attacked by pathogens develop immunity using processes and mechanisms corresponding to those operating in animals. Last, but not least, both animals and plants use the same molecules and pathways to drive their circadian rhythms. Currently, owing to the critical mass of new data which has accumulated, plant science has reached a crossroads culminating in the emergence of plant neurobiology as the most recent area of plant sciences. Plants perform complex information processing and use not only action potentials but also synaptic modes of cell–cell communication. Thus, the term ‘plant neurobiology’ appears to be justified. In fact, the word neuron was taken by animal neurobiologists from Greek, where the original meaning of this word is vegetal fibre. Several surprises emerge when applying a ‘neurobiological’ perspective to illustrate how the plant tissues and the plant body are organized. Firstly, root apices are specialized not only for the uptake of nutrients but they also seem to support neuronal-like activities Proofbased on plant synapses. These synapses transport auxin via synaptic processes, suggesting that auxin is a plant-specific neurotransmitter. Altogether, root apices emerge as command centres and represent the anterior pole of the plant body.
    [Show full text]
  • Lesson Sample Grade 4
    Lesson Sample Grade 4 Plant and Animal Structures A New Generation ® Materials List Needed from the kit Provided by the teacher 96 bean seeds 9 celery stalks 1 bottle of clove oil 30 glue sticks 1 bottle of food coloring 30 individually wrapped hard candies 1 bottle of peppermint oil 60 jelly beans 2 bunches of model lilies 31 lab aprons 8 cardboard tubes 1 large container 9 clothespins 3 large trash bags 40 cotton balls 30 living flowers 1 Cow Eye Dissection Mat 1 pair of sharp scissors 8 flat marbles 30 pairs of scissors 21 foam trays 8 paper clips 30 hand lenses 30 permanent markers 9 large plastic cups 60 potato chips 13 large resealable plastic bags 8 rolls of clear tape 1 Literacy Series Reader: Plant and Animal 30 rulers, 30 cm Structures 32 sheets of paper 30 medium resealable plastic bags 8 towels (optional) 30 paper bags 2 gal water 3 plastic tanks, 1 gal Additional materials brought from home (for eye 32 small plastic cups models, optional) 126 pairs of disposable gloves Chart paper 8 pairs of dissection scissors Crayons, markers, or colored pencils 8 pairs of forceps Darkened classroom 1 pair of safety goggles, large Disinfectant cleaner 30 pairs of safety goggles, small Light source or brightly lit window 8 penlights Markers 1 Plant and Animal Structures Photo Card Set Paper towels (for cleanup) 1 Preserved Package Projection system (optional) 10 squids Sunlit window or other warm area 2 cow eyes Various craft materials 1 sheep brain 1 roll of aluminum foil Provided by the student 1 roll of paper towels 1 science notebook 1 roll of wax paper 16 rubber bands 1 scalpel 24 small resealable plastic bags 8 Squid Dissection Mats 8 thumbtacks Playfoam® Radish seeds Sandpaper BUILDING BLOCKS OF SCIENCE Plant and Animal Structures A New Generation Teacher’s Guide Unit and Lesson Summaries Unit Overview Plant and Animal Structures introduces students to a variety of internal and external structures of plants and animals using a variety of activities including animal and plant dissections and models.
    [Show full text]
  • 29 | Vertebrates 791 29 | VERTEBRATES
    Chapter 29 | Vertebrates 791 29 | VERTEBRATES Figure 29.1 Examples of critically endangered vertebrate species include (a) the Siberian tiger (Panthera tigris), (b) the mountain gorilla (Gorilla beringei), and (c) the Philippine eagle (Pithecophega jefferyi). (credit a: modification of work by Dave Pape; credit b: modification of work by Dave Proffer; credit c: modification of work by "cuatrok77"/Flickr) Chapter Outline 29.1: Chordates 29.2: Fishes 29.3: AmphiBians 29.4: Reptiles 29.5: Birds 29.6: Mammals 29.7: The Evolution of Primates Introduction Vertebrates are among the most recognizable organisms of the animal kingdom. More than 62,000 vertebrate species have been identified. The vertebrate species now living represent only a small portion of the vertebrates that have existed. The best-known extinct vertebrates are the dinosaurs, a unique group of reptiles, which reached sizes not seen before or after in terrestrial animals. They were the dominant terrestrial animals for 150 million years, until they died out in a mass extinction near the end of the Cretaceous period. Although it is not known with certainty what caused their extinction, a great deal is known about the anatomy of the dinosaurs, given the preservation of skeletal elements in the fossil record. Currently, a number of vertebrate species face extinction primarily due to habitat loss and pollution. According to the International Union for the Conservation of Nature, more than 6,000 vertebrate species are classified as threatened. Amphibians and mammals are the classes with the greatest percentage of threatened species, with 29 percent of all amphibians and 21 percent of all mammals classified as threatened.
    [Show full text]
  • Canalization in Evolutionary Genetics: a Stabilizing Theory?
    Problems and paradigms Canalization in evolutionary genetics: a stabilizing theory? Greg Gibson1* and GuÈ nter Wagner2 ``The stability of the morphogenetic system is destroyed (rendered labile) due either to variation in environmental factors or to mutation. On the other hand, in the course of evolution stability is reestablished by the continuous action of stabilizing selection. Stabilizing selection produces a stable form by creating a regulating apparatus. This protects normal morphogenesis against possible disturbances by chance variation in the external environment and also against small variations in internal factors (i.e. mutations). In this case, natural selection is based upon the selective advantage of the norm (often the new norm) over any deviations from it.'' I.I. Schmalhausen, 1949 (p 79 of 1986 reprinted edition). Summary mechanisms that produce it, and that it has implications for Canalization is an elusive concept. The notion that both developmental and evolutionary biology.(4) However, biological systems ought to evolve to a state of higher stability against mutational and environmental perturba- evolutionary geneticists have devised a more limited mean- tions seems simple enough, but has been exceedingly ing for the term canalization. Whereas buffering refers to difficult to prove. Part of the problem has been the lack keeping a trait constant and hence to low variance about of a definition of canalization that incorporates an the mean, the associated evolutionary questions are whether evolutionary genetic perspective and provides a frame- or not traits can evolve such that they become less likely to work for both mathematical and empirical study. After briefly reviewing the importance of canalization in vary, and if so, whether particular ones have done so, and studies of evolution and development, we aim, with eventually to address how this has occurred.
    [Show full text]
  • The Body Plan Concept and Its Centrality in Evo-Devo
    Evo Edu Outreach (2012) 5:219–230 DOI 10.1007/s12052-012-0424-z EVO-DEVO The Body Plan Concept and Its Centrality in Evo-Devo Katherine E. Willmore Published online: 14 June 2012 # Springer Science+Business Media, LLC 2012 Abstract A body plan is a suite of characters shared by a by Joseph Henry Woodger in 1945, and means ground plan group of phylogenetically related animals at some point or structural plan (Hall 1999; Rieppel 2006; Woodger 1945). during their development. The concept of bauplane, or body Essentially, a body plan is a suite of characters shared by a plans, has played and continues to play a central role in the group of phylogenetically related animals at some point study of evolutionary developmental biology (evo-devo). during their development. However, long before the term Despite the importance of the body plan concept in evo- body plan was coined, its importance was demonstrated in devo, many researchers may not be familiar with the pro- research programs that presaged the field of evo-devo, per- gression of ideas that have led to our current understanding haps most famously (though erroneously) by Ernst Haeck- of body plans, and/or current research on the origin and el’s recapitulation theory. Since the rise of evo-devo as an maintenance of body plans. This lack of familiarity, as well independent field of study, the body plan concept has as former ties between the body plan concept and metaphys- formed the backbone upon which much of the current re- ical ideology is likely responsible for our underappreciation search is anchored.
    [Show full text]
  • Phenotypic Plasticity and Modularity Allow for the Production of Novel
    Londe et al. EvoDevo (2015) 6:36 DOI 10.1186/s13227-015-0031-5 EvoDevo RESEARCH Open Access Phenotypic plasticity and modularity allow for the production of novel mosaic phenotypes in ants Sylvain Londe1*, Thibaud Monnin1, Raphaël Cornette2, Vincent Debat2, Brian L. Fisher3 and Mathieu Molet1 Abstract Background: The origin of discrete novelties remains unclear. Some authors suggest that qualitative phenotypic changes may result from the reorganization of preexisting phenotypic traits during development (i.e., developmental recombination) following genetic or environmental changes. Because ants combine high modularity with extreme phenotypic plasticity (queen and worker castes), their diversified castes could have evolved by developmental recombination. We performed a quantitative morphometric study to investigate the developmental origins of novel phenotypes in the ant Mystrium rogeri, which occasionally produces anomalous ‘intercastes.’ Our analysis compared the variation of six morphological modules with body size using a large sample of intercastes. Results: We confirmed that intercastes are conspicuous mosaics that recombine queen and worker modules. In addition, we found that many other individuals traditionally classified as workers or queens also exhibit some level of mosaicism. The six modules had distinct profiles of variation suggesting that each module responds differentially to factors that control body size and polyphenism. Mosaicism appears to result from each module responding differently yet in an ordered and predictable manner to intermediate levels of inducing factors that control polyphenism. The order of module response determines which mosaic combinations are produced. Conclusions: Because the frequency of mosaics and their canalization around a particular phenotype may evolve by selection on standing genetic variation that affects the plastic response (i.e., genetic accommodation), develop- mental recombination is likely to play an important role in the evolution of novel castes in ants.
    [Show full text]